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Can Heritable Epigenetic Variation Aid Speciation? Hindawi Publishing Corporation Genetics Research International Volume 2012, Article ID 698421, 9 pages doi:10.1155/2012/698421 Review Article Environmental Heterogeneity and Phenotypic Divergence: Can Heritable Epigenetic Variation Aid Speciation? Ruth Flatscher,1, 2 Bozoˇ Frajman,1 Peter Schonswetter,¨ 1 and Ovidiu Paun2 1 Institute of Botany, University of Innsbruck, Sternwartestraße 15, 6020 Innsbruck, Austria 2 Department of Systematic and Evolutionary Botany, University of Vienna, Rennweg 14, 1030 Vienna, Austria Correspondence should be addressed to Ovidiu Paun, [email protected] Received 22 August 2011; Revised 7 November 2011; Accepted 23 November 2011 Academic Editor: Christina L. Richards Copyright © 2012 Ruth Flatscher et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. The dualism of genetic predisposition and environmental influences, their interactions, and respective roles in shaping the phenotype have been a hot topic in biological sciences for more than two centuries. Heritable epigenetic variation mediates between relatively slowly accumulating mutations in the DNA sequence and ephemeral adaptive responses to stress, thereby providing mechanisms for achieving stable, but potentially rapidly evolving phenotypic diversity as a response to environmental stimuli. This suggests that heritable epigenetic signals can play an important role in evolutionary processes, but so far this hypothesis has not been rigorously tested. A promising new area of research focuses on the interaction between the different molecular levels that produce phenotypic variation in wild, closely-related taxa that lack genome-wide genetic differentiation. By pinpointing specific adaptive traits and investigating the mechanisms responsible for phenotypic differentiation, such study systems could allow profound insights into the role of epigenetics in the evolution and stabilization of phenotypic discontinuities, and could add to our understanding of adaptive strategies to diverse environmental conditions and their dynamics. 1. Introduction of biological variation: the genetic system defines the range of functional possibilities of each individual. However, Patterns and causes of biological variation have fascinated these heritable differences translate into the phenotype and challenged natural scientists for a long time. The only indirectly via the resulting RNA and protein products Darwinian evolutionary theory highlights the importance which mould the structure and function of an organism. of natural variation as raw material upon which selection Much progress has been made in recent years in identifying processes can act, thereby increasing the fitness of locally gene functions and candidate genes coding for important adapted phenotypes [1]. Conceptual and technical develop- metabolic enzymes, but analyses of whole genomes remain a ments since the late 19th century have greatly enhanced our complex challenge. Even in organisms whose whole genome understanding of some of the main mechanisms producing is sequenced, a large number of genes still remain unchar- and maintaining biological variation, namely, genetic muta- acterized [8]. The second important source of biological tion and recombination [2]. However, natural selection acts variation is fluctuation in rates of gene expression, resulting upon phenotypic variation represented by the individual [3], in phenotypic plasticity [9, 10]. Genes can be up- or down- which is delimited by its genetic constitution, but also shaped regulated in response to environmental conditions, such as by its specific environment [4] and developmental processes temperature regimes or water supply, or intrinsic factors [5]. The process of evolution is thus a result of complex such as specific phenological or developmental stages [11]. interactions between various intrinsic and extrinsic factors This leads to temporary modifications of the phenotype, [6]. which are generally not passed on to the next generation [12, Therefore, current evolutionary investigations should 13]. The third level, heritable epigenetic variation, via both consider several levels of biological variation [7]. First, specialized enzymology inducing structural modifications of differences in the DNA sequence account for a great amount the DNA (through DNA methylation, histone acetylation 2 Genetics Research International [14, 15]) and small interfering (si) RNA populations [16, 17], lacking genetic variability [45] and/or occupying a frag- results in (meta) stable chromatin landscape differences. mented landscape. Selectable epigenetic variation can enable Epigenetic differences determine if and where particular genetically depauperate lineages to adapt [46] until genetic genes or groups of genes are to be expressed, while the under- assimilation occurs (i.e., when environmentally induced lying DNA sequence remains identical [18]. Most of these phenotypic variation becomes fixed by secondary genetic differences are reversible developmental effects and they control, e.g., after deamination of methylated cytosine to are part of the molecular processes underlying phenotypic thymine [13, 47]). Thus, heritable epigenetic variation could plasticity in response to variation in the environment [19]. pave the way for genetic adaptation. However, environmental change, severe stress or genomic The epigenetic sources of variation can be stochastic shock events like hybridization or genome duplication can epimutations, but a major part of the epigenetic variation change the epigenetic configuration of an organism resulting is triggered by stress or changes in the environment [3, in new phenotypes [20–26], and some of these alterations 22, 48], that is, under circumstances when new phenotypes can be passed on to the next generations [27–30]. could be crucial for survival. Moreover, if conditions return The molecular mechanisms underlying these compo- to their original state, spontaneous back-mutation of epi- nents of phenotypic variation differ in their stability and in alleles can restore original phenotypes (e.g., in position- the time frames in which they confer phenotypic novelty. The effect variegation [27]). In the light of epigenetic variation, genetic sequence is the most stable, evolving slowly through the involvement of the environment in evolution becomes mutation and gradually accumulating changes over a large twofold: as a stimulant of variation and as the selector of number of generations. In contrast, gene expression levels adaptive variation. can be rapidly and continuously regulated within a very At the interface between genotype and environment, the short time [11], much shorter than the generation length of overall rate of epimutations is often much higher than that an organism, and allow an almost instantaneous response of genetic mutations [49], resulting in a more dynamic level of the individual to its environment within limits defined of variation. Novel epigenetic modifications may originate by its genetic constitution. Heritable epigenetic alterations simultaneously in several individuals in a population under act within an intermediate time horizon, since they can stress, which will facilitate fixation. Despite the potentially occurasanimmediateandmultilocusreactiontodifferent high loss of epigenetic novelties by epigenetic reset [19], kinds of external or intrinsic stimuli [23] but are not as epimutations can reach equilibrium frequencies within pop- ephemeral as plastic gene regulation and can affect the ulations rapidly, over less than a dozen generations if the following generations [18]. environmental stress is maintained long enough [28]. In It has long been established that mutations in DNA stark contrast to the expected incidence of genetic mutations, sequence are the primary raw material for evolutionary environmental fluctuations can trigger multiple epimuta- change [2]. The involvement of environmental influences tions in the same individual. This renders fast ecological in generating heritable biological variation is still debated adaptation affecting (complex) adaptive traits more plausible [13, 22], as is the necessity of extending our modern [50]. Hence, recombination is not necessarily a prerequisite evolutionary synthesis [31]. Accumulating evidence indicates for adaptive change, if the latter is driven from the epigenetic that modifications of epigenetic signals are correlated with level. In addition, epigenetic mechanisms may partly defy phenotypic variation within and among species [25, 32– well-understood population processes, such as allelic drift 34], placing epigenetic differentiation even in a macroevolu- (due to potential maintenance of relatively constant epiallelic tionary context. Latest developments regarding the potential frequencies through environmental influence). Being more role of phenotypic plasticity in driving diversification and flexible and dynamic than DNA sequence information, speciation have been discussed elsewhere (e.g., [13, 35]). We variation in epigenetic signals could therefore act as major are hereafter focusing on the impact of heritable epigenetic driving force in rapid adaptive processes. variation on the process of evolution and propose a research Epigenetic variation can have extensive consequences, plan to address its evolutionary significance. even in the absence of genetic variability [45, 50, 51]. Epigenetics may introduce,
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